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Effect of Different Carbon Substrates on the Removal of Hexahydro-1,3,5-Trinitro-1,3,5-Triazine (RDX) and Octahydro-1,3,5,7-Tetranitro-1,3,5,7-Tetrazocine (HMX) by Anaerobic Mesophilic Granular Sludge

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Abstract

The influence of carbon substrate supplement on the degradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) and octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine (HMX) by anaerobic mesophilic granular sludge was investigated. Batch experiments were carried to evaluate the biodegradation performance in the presence of acetate, ethanol, glucose and soluble starch. The results of specific methanogenic activity tests showed that RDX and HMX at concentration of 139 and 20 μmol L−1, respectively, had no major inhibitory effect on the bioactivity of anaerobic granular sludge. Glucose and acetate could better facilitate the degradation of RDX and HMX when compared with ethanol and soluble starch. The concentration of carbon substrate was considered critical for enhancing the transformation of RDX and HMX. As carbon substrate concentration increased up to 50 mmol chemical oxygen demand (COD) L−1, there was a major stimulatory effect of the amended carbon substrates, while a slight inhibitory effect was also found at some concentrations. These results indicate that adding suitable carbon substrates may be an important strategy for stimulating the anaerobic biotransformation of high-energetic ammunition compounds in bioreactors.

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References

  • Adrian, N. R., & Arnett, C. M. (2006). Hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) serves as a carbon and energy source for a mixed culture under anaerobic conditions. Current Microbiology, 53, 129–134.

    Article  CAS  Google Scholar 

  • Adrian, N. R., Arnett, C. M., & Hickey, R. F. (2003). Stimulating the anaerobic biodegradation of explosives by the addition of hydrogen or electron donors that produce hydrogen. Water Research, 37, 3499–3507.

    Article  CAS  Google Scholar 

  • An, C. J., He, Y. L., Huang, G. H., & Liu, Y. H. (2010a). Performance of mesophilic anaerobic granules for removal of octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine (HMX) from aqueous solution. Journal of Hazardous Materials, 179, 526–532.

    Article  CAS  Google Scholar 

  • An, C. J., He, Y. L., Huang, G. H., & Yang, S. C. (2010b). Degradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by anaerobic mesophilic granular sludge from a UASB reactor. Journal of Chemical Technology and Biotechnology, 85, 831–838.

    Article  CAS  Google Scholar 

  • Annamaria, H., Manno, D., Strand, S. E., Bruce, N. C., & Hawari, J. (2010). Biodegradation of RDX and MNX with Rhodococcus sp. strain DN22: new insights into the degradation pathway. Environmental Science & Technology, 44, 9330–9336.

    Article  CAS  Google Scholar 

  • APHA. (1998). Standard methods for the examination of water and wastewater. Washington, DC: American Public Health Association.

    Google Scholar 

  • Astratinei, V., van Hullebusch, E., & Lens, P. (2006). Bioconversion of selenate in methanogenic anaerobic granular sludge. Journal of Environmental Quality, 35, 1873–1883.

    Article  CAS  Google Scholar 

  • Aulenta, F., Gossett, J. M., Papini, M. P., Rossetti, S., & Majone, M. (2005). Comparative study of methanol, butyrate, and hydrogen as electron donors for long-term dechlorination of tetrachloroethene in mixed anerobic cultures. Biotechnology and Bioengineering, 91, 743–753.

    Article  CAS  Google Scholar 

  • Baczynski, T. P., Grotenhuis, T., & Knipscheer, P. (2004). The dechlorination of cyclodiene pesticides by methanogenic granular sludge. Chemosphere, 55, 653–659.

    Article  CAS  Google Scholar 

  • Beller, H. R. (2002). Anaerobic biotransformation of RDX (hexahydro-1,3,5-trinitro-1,3,5-triazine) by aquifer bacteria using hydrogen as the sole electron donor. Water Research, 36, 2533–2540.

    Article  CAS  Google Scholar 

  • Bhatt, M., Zhao, J. S., Halasz, A., & Hawari, J. (2006). Biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine by novel fungi isolated from unexploded ordnance contaminated marine sediment. Journal of Industrial Microbiology & Biotechnology, 33, 850–858.

    Article  CAS  Google Scholar 

  • Boopathy, R. (2001). Enhanced biodegradation of cyclotetramethylenetetranitramine (HMX) under mixed electron-acceptor condition. Bioresource Technology, 76, 241–244.

    Article  CAS  Google Scholar 

  • Chen, D., Liu, Z. L., & Banwart, W. (2011). Concentration-dependent RDX uptake and remediation by crop plants. Environmental Science and Pollution Research, 18, 908–917.

    Article  CAS  Google Scholar 

  • Chipasa, K. B., & Mędrzycka, K. (2006). Behavior of lipids in biological wastewater treatment processes. Journal of Industrial Microbiology and Biotechnology, 33, 635–645.

    Article  CAS  Google Scholar 

  • Collins, G., Foy, C., McHugh, S., & O’ Flaherty, V. (2005). Anaerobic treatment of 2,4,6-trichlorophenol in an expanded granular sludge bed-anaerobic filter (EGSB-AF) bioreactor at 15 °C. FEMS Microbiology Ecology, 53, 167–178.

    Article  CAS  Google Scholar 

  • Doong, R. A., & Chang, S. M. (2000). Relationship between electron donor and microorganism on the dechlorination of carbon tetrachloride by an anaerobic enrichment culture. Chemosphere, 40, 1427–1433.

    Article  CAS  Google Scholar 

  • Doong, R. A., & Chen, T. F. (1996). Anaerobic degradation of 1,1,1-trichloroethane with the amendment of different substrate and microbial concentrations. Chemosphere, 32, 2003–2014.

    Article  CAS  Google Scholar 

  • dos Santos, A. B., Cervantes, F. J., & van Lier, J. B. (2004). Azo dye reduction by thermophilic anaerobic granular sludge, and the impact of the redox mediator anthraquinone-2,6-disulfonate (AQDS) on the reductive biochemical transformation. Applied Microbiology and Biotechnology, 64, 62–69.

    Article  Google Scholar 

  • Fiorella, P. D., & Spain, J. C. (1997). Transformation of 2,4,6-trinitrotoluene by Pseudomonas pseudoalcaligenes JS52. Applied and Environmental Microbiology, 63, 2007–2015.

    CAS  Google Scholar 

  • Gnanapragasam, G., Senthilkumar, M., Arutchelvan, V., Velayutham, T., & Nagarajan, S. (2011). Bio-kinetic analysis on treatment of textile dye wastewater using anaerobic batch reactor. Bioresource Technology, 102, 627–632.

    Article  CAS  Google Scholar 

  • Hamer, G. (1997). Microbial consortia for multiple pollutant biodegradation. Pure and Applied Chemistry, 69, 2343–2356.

    Article  CAS  Google Scholar 

  • He, J. Z., Sung, Y., Dollhopf, M. E., Fathepure, B. Z., Tiedje, J. M., & Loffler, F. E. (2002). Acetate versus hydrogen as direct electron donors to stimulate the microbial reductive dechlorination process at chloroethene-contaminated sites. Environmental Science & Technology, 36, 3945–3952.

    Article  CAS  Google Scholar 

  • Hwang, P., Chow, T., & Adrian, N. R. (2000). Transformation of trinitrotoluene to triaminotoluene by mixed cultures incubated under methanogenic conditions. Environmental Toxicology and Chemistry, 19, 836–841.

    Article  CAS  Google Scholar 

  • Jayamani, I., Manzella, M., & Cupples, A. (2013). RDX degradation potential in soils previously unexposed to RDX and the identification of RDX-degrading species in one agricultural soil using stable isotope probing. Water, Air, and Soil Pollution, 224, 1–15.

    Article  CAS  Google Scholar 

  • Kanekar, S. P., Kanekar, P. P., Sarnaik, S. S., Gujrathi, N. P., Shede, P. N., Kedargol, M. R., & Reardon, K. F. (2009). Bioremediation of nitroexplosive wastewater by an yeast isolate Pichia sydowiorum MCM Y-3 in fixed film bioreactor. Journal of Industrial Microbiology & Biotechnology, 36, 253–260.

    Article  CAS  Google Scholar 

  • Lettinga, G., Vanvelsen, A. F. M., Hobma, S. W., Dezeeuw, W., & Klapwijk, A. (1980). Use of the upflow sludge blanket (USB) reactor concept for biological wastewater-treatment, especially for anaerobic treatment. Biotechnology and Bioengineering, 22, 699–734.

    Article  CAS  Google Scholar 

  • Lim, S. J., & Kim, T.-H. (2014). Applicability and trends of anaerobic granular sludge treatment processes. Biomass and Bioenergy, 60, 189–202.

    Article  CAS  Google Scholar 

  • Liu, Y. H., He, Y. L., Yang, S. C., & An, C. J. (2006). Studies on the expansion characteristics of the granular bed present in EGSB bioreactors. Water SA, 32, 555–560.

    Google Scholar 

  • Liu, Q. L., Yan, X. H., Yin, X. M., Situ, B., Zhou, H. K., Lin, L., Li, B., Gan, N., & Zheng, L. (2013). Electrochemical enzyme-linked immunosorbent assay (ELISA) for alpha-fetoprotein based on glucose detection with multienzyme-nanoparticle amplification. Molecules, 18, 12675–12686.

    Article  CAS  Google Scholar 

  • Lovanh, N., & Alvarez, P. J. J. (2004). Effect of ethanol, acetate, and phenol on toluene degradation activity and tod-lux expression in Pseudomonas putida TOD102: evaluation of the metabolic flux dilution model. Biotechnology and Bioengineering, 86, 801–808.

    Article  CAS  Google Scholar 

  • Lozano, C. J. S., Mendoza, M. V., de Arango, M. C., & Monroy, E. F. C. (2009). Microbiological characterization and specific methanogenic activity of anaerobe sludges used in urban solid waste treatment. Waste Management, 29, 704–711.

    Article  CAS  Google Scholar 

  • Mamma, D., Kalogeris, E., Papadopoulos, N., Hatzinikolaou, D. G., Christrakopoulos, P., & Kekos, D. (2004). Biodegradation of phenol by acclimatized Pseudomonas putida cells using glucose as an added growth substrate. Journal of Environmental Science and Health Part A-Toxic/Hazardous Substances & Environmental Engineering, 39, 2093–2104.

    Article  Google Scholar 

  • Mukhi, S., Pan, X., Cobb, G. P., & Patiño, R. (2005). Toxicity of hexahydro-1,3,5-trinitro-1,3,5-triazine to larval zebrafish (Danio rerio). Chemosphere, 61, 178–185.

    Article  CAS  Google Scholar 

  • Oh, B. T., & Alvarez, P. J. J. (2002). Hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) degradation in biologically-active iron columns. Water, Air, and Soil Pollution, 141, 325–335.

    Article  CAS  Google Scholar 

  • Oh, B. T., Just, C. L., & Alvarez, P. J. J. (2001). Hexahydro-1,3,5-trinitro-1,3,5-triazine mineralization by zerovalent iron and mixed anaerobic cultures. Environmental Science & Technology, 35, 4341–4346.

    Article  CAS  Google Scholar 

  • Oh, S. Y., Chiu, P. C., Kim, B. J., & Cha, D. K. (2003). Enhancing Fenton oxidation of TNT and RDX through pretreatment with zero-valent iron. Water Research, 37, 4275–4283.

    Article  CAS  Google Scholar 

  • Rooney-Varga, J. N., Anderson, R. T., Fraga, J. L., Ringelberg, D., & Lovley, D. R. (1999). Microbial communities associated with anaerobic benzene degradation in a petroleum-contaminated aquifer. Applied and Environmental Microbiology, 65, 3056–3063.

    CAS  Google Scholar 

  • Ryan, P., Forbes, C., McHugh, S., O’Reilly, C., Fleming, G. T. A., & Colleran, E. (2010). Enrichment of acetogenic bacteria in high rate anaerobic reactors under mesophilic and thermophilic conditions. Water Research, 44, 4261–4269.

    Article  CAS  Google Scholar 

  • Shen, D. S., Liu, X. W., & Feng, H. J. (2005). Effect of easily degradable substrate on anaerobic degradation of pentachlorophenol in an upflow anaerobic sludge blanket (UASB) reactor. Journal of Hazardous Materials, 119, 239–243.

    Article  CAS  Google Scholar 

  • Sherburne, L. A., Shrout, J. D., & Alvarez, P. J. J. (2005). Hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) degradation by Acetobacterium paludosum. Biodegradation, 16, 539–547.

    Article  CAS  Google Scholar 

  • Song, K. S., Li, L., Tedesco, L., Duan, H. T., Li, L. H., & Du, J. (2014). Remote quantification of total suspended matter through empirical approaches for inland waters. Journal of Environmental Informatics, 23, 23–36.

    Article  CAS  Google Scholar 

  • Sørensen, A., & Ahring, B. (1993). Measurements of the specific methanogenic activity of anaerobic digestor biomass. Applied Microbiology and Biotechnology, 40, 427–431.

    Article  Google Scholar 

  • Tay, J. H., He, Y. X., & Yan, Y. G. (2001). Improved anaerobic degradation of phenol with supplemental glucose. Journal of Environmental Engineering-ASCE, 127, 38–45.

    Article  CAS  Google Scholar 

  • Thompson, K. T., Crocker, F. H., & Fredrickson, H. L. (2005). Mineralization of the cyclic nitramine explosive hexahydro-1,3,5-trinitro-1,3,5-triazine by Gordonia and Williamsia spp. Applied and Environmental Microbiology, 71, 8265–8272.

    Article  CAS  Google Scholar 

  • Upadhyay, U., Kumar, P., & Mehrotra, I. (2008). Anaerobic degradation of benzoate: batch studies. Bioresource Technology, 99, 6861–6865.

    Article  CAS  Google Scholar 

  • US EPA. (2004). 2004 Edition of the drinking water standards and health advisories, Office of Water US Environmental Protection Agency Washington, DC. http://water.epa.gov/action/advisories/drinking/upload/2009_04_27_criteria_drinking_dwstandards2004.pdf. Accessed 14 July 2014.

  • Wang, C. C., Lee, C. M., Lu, C. J., Chuang, M. S., & Huang, C. Z. (2000). Biodegradation of 2,4,6-trichlorophenol in the presence of primary substrate by immobilized pure culture bacteria. Chemosphere, 41, 1873–1879.

    Article  CAS  Google Scholar 

  • Wang, N. D., Peng, J., & Hill, G. (2002). Biochemical model of glucose induced enhanced biological phosphorus removal under anaerobic condition. Water Research, 36, 49–58.

    Article  CAS  Google Scholar 

  • Wijetunga, S., Li, X. F., & Jian, C. (2010). Effect of organic load on decolourization of textile wastewater containing acid dyes in upflow anaerobic sludge blanket reactor. Journal of Hazardous Materials, 177, 792–798.

    Article  CAS  Google Scholar 

  • Wu, W. M., Bhatnagar, L., & Zeikus, J. G. (1993). Performance of anaerobic granules for degradation of pentachlorophenol. Applied and Environmental Microbiology, 59, 389–397.

    CAS  Google Scholar 

  • Yang, Q., Shang, H. T., Wang, X. L., Li, H. D., & Wang, J. L. (2006). Anaerobic degradation of tetrachloroethylene using different co-substrates as electron donors. Biomedical and Environmental Sciences, 19, 73–76.

    CAS  Google Scholar 

  • Yang, S., He, Y., Liu, Y., Chou, C., Zhang, P., & Wang, D. (2010). Effect of wastewater composition on the calcium carbonate precipitation in upflow anaerobic sludge blanket reactors. Frontiers of Environmental Science & Engineering in China, 4, 142–149.

    Article  Google Scholar 

  • Zhao, J. S., Paquet, L., Halasz, A., Manno, D., & Hawari, M. (2004). Metabolism of octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine by Clostridium bifermentans strain HAW-1 and several other H2-producing fermentative anaerobic bacteria. FEMS Microbiology Letters, 237, 65–72.

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by the Natural Science and Engineering Research Council of Canada and the Canada Foundation for Innovation. The authors are also grateful to the editors and the anonymous reviewers for their insightful comments and suggestions.

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Correspondence to Guohe Huang.

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An, C., Shi, Y., He, Y. et al. Effect of Different Carbon Substrates on the Removal of Hexahydro-1,3,5-Trinitro-1,3,5-Triazine (RDX) and Octahydro-1,3,5,7-Tetranitro-1,3,5,7-Tetrazocine (HMX) by Anaerobic Mesophilic Granular Sludge. Water Air Soil Pollut 225, 2174 (2014). https://doi.org/10.1007/s11270-014-2174-8

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